Sniffing (behavior)

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Two dogs sniffing each other Dogs sniffing each other.jpg
Two dogs sniffing each other

Sniffing is a perceptually-relevant behavior, defined as the active sampling of odors through the nasal cavity for the purpose of information acquisition. This behavior, displayed by all terrestrial vertebrates, is typically identified based upon changes in respiratory frequency and/or amplitude, [1] [2] and is often studied in the context of odor guided behaviors and olfactory perceptual tasks. Sniffing is quantified by measuring intra-nasal pressure or flow or air [3] [4] [5] [6] or, while less accurate, through a strain gauge on the chest to measure total respiratory volume. [7] Strategies for sniffing behavior vary depending upon the animal, with small animals (rats, mice, hamsters) displaying sniffing frequencies ranging from 4 to 12 Hz [2] [3] [8] but larger animals (humans) sniffing at much lower frequencies, usually less than 2 Hz. [7] [9] Subserving sniffing behaviors, evidence for an "olfactomotor" circuit in the brain exists, [10] [11] wherein perception or expectation of an odor can trigger brain respiratory center to allow for the modulation of sniffing frequency and amplitude and thus acquisition of odor information. Sniffing is analogous to other stimulus sampling behaviors, including visual saccades, active touch, and whisker movements in small animals (viz., whisking). [12] [13] Atypical sniffing has been reported in cases of neurological disorders, especially those disorders characterized by impaired motor function and olfactory perception. [14] [15]

Contents

Background and history of sniffing

An island fox sniffing the ground and scent marking

Background

The behavior of sniffing incorporates changes in air flow within the nose. This can involve changes in the depth of inhalation and the frequency of inhalations. Both of these entail modulations in the manner whereby air flows within the nasal cavity and through the nostrils. As a consequence, when the air being breathed is odorized, odors can enter and leave the nasal cavity with each sniff. The same applies regardless of what gas is being inhaled, including toxins and solvents, and other industrial chemicals which may be inhaled as a form of drug or substance abuse. [16]

The act of sniffing is considered distinct from respiration on several grounds. In humans, one can assess the occurrence of a sniff based upon volitional control of air movement through the nose. [17] In these cases, human subjects can be asked to inhale for a certain amount of time, or in a particular pattern. [7] Some animals are obligate nasal breathers, wherein the only air for respiration must arrive into the lungs via the nose. This includes rats and mice. Thus, in these animals the distinction between a breath and a sniff is not clear and could be argued to be indistinguishable. [18] (See sniffing in small animals.)

Sniffing is observed among all terrestrial vertebrates, wherein they inhale environmental air. [19] Sniffing may also occur in underwater environments wherein an animal may exhale air from within its lungs and nasal cavity to acquire odors within an aquatic environment and then re-inhale this air. [20] (See sniffing in small animals.)

While sniffing behavior is often observed and discussed within the context of acquiring odor information, sniffing is also displayed during the performance of motivated behaviors and upon deep brain electrical stimulation of brain reward centers. For instance, prior to obtaining a food reward, mice and rabbits increase their sniffing frequency [3] [21] in a manner independent of seeking odor information. Sniffing behavior is also displayed by animals upon involuntary electrical stimulation of numerous brain structures. [22] Thus, while sniffing is often considered a critical part of olfaction, its link with motivated and reward behaviors suggests it plays a role in other behaviors.

History

Studies into the perceptual correlates of sniffing on human olfaction did not reach the mainstream scientific community until the 1950s. Frank Jones, an American psychologist, published a paper demonstrating the interplay between parameters of sniffing and odor detection thresholds. He found that deep sniffs, consisting of a large volume of air, allowed for consistent and accurate detection of odors. [23]

One of the earliest reports of exploring sniffing in non-human animals was provided by Welker in his 1964 article, Analysis of sniffing in the albino rat. [1] In this study, Welker used video recordings of rats during presentation with odors and other stimuli to explore the chest movements as an index of sniffing. This was the first paper to report that rats can sniff at frequencies reaching 12 Hz upon detection of odors and during free exploration. This paper also provided early evidence that the rhythm of sniffing was coupled with other sensory behaviors, such as whisking, or the movement of the whiskers.

While behavioral and psycho-physical studies into sniffing and its influence on odor perception began to surface, much less work was being performed to explore the influence of sniffing behaviors on the physiological processing of odors within the brain. Early recordings from the olfactory bulbs of hedgehogs by Lord Edgar Adrian, who previously won the 1932 Nobel Prize along with Sir Charles Sherrington for their work on the functions of neurons, revealed that neural oscillations within the hedgehog olfactory bulb were entrained to the respiratory cycle. [24] Further, odor-evoked oscillations (including an exhaled puff from a pipe), were amplified along with the respiratory cycle. These data gave evidence that information processing within the brain, particularly that of odors, was linked with respiration - establishing the integral nature of sniffing for the physiological processing of odors. About 20 years later, Max Mozell published a series of studies wherein he further proposed that the flow rate and the sorption properties of odorants interplay to affect the location of odorant binding to olfactory receptor neurons in the nose and consequentially odor input to the brain. [25] Later, evidence that single neurons in the olfactory bulb, the brain's first relay station for odor information, are entrained with respiration was presented, establishing a solid basis for the control of odor input to the brain and the processing of odors by sniffing. [26]

Methods for quantifying sniffing

There are multiple methods available for measuring sniffing. While these methods are applicable for most animal models (mice to humans), selection of appropriate sniff measurement methods should be determined by experimental need for precision.

Video

Perhaps the simplest method for determining the moment of sniffing is video-based. High resolution video of small animals (e.g., rats) during immobile respiration enables approximations of sniffing, including identification of individual sniff events. [1] Similar methods can be employed to identify fast, high frequency sniffing during states of arousal and stimulus investigation. [1] This method, however, does not provide direct evidence for sniffing and is not reliable in larger animals (rabbits to humans).

Chest strain

Sensors to measure chest expansion during inhalation provide direct information of sniff cycles. [27] These methods include mechanical and optical devices. Mechanical devices for sniffing measurements are piezo foils placed under the chests of small animals and strain gauge around the chests of larger animals. In both cases, a positive increase in signal output (voltage) can be identified and used to index inhalation events. Alternatively, a photo transducer can be placed on the opposite side of an animal's chest from a light source (e.g., a Light-emitting diode). In this design, a decrease in signal reflects inhalation (chest expansion) as the chest would interrupt the light passage to the photo transducer.

Nasal microphone

As a direct measurement of sniffing, early studies favored the use of microphones placed/secured external to the anterior nares, the external openings of the nasal cavity. This method has advantages to directly index air leaving the nares (increase in microphone output), yet is mostly non-invasive. Due to this non-invasive nature of microphone measures, these methods have been employed in dogs during odor tracking exercises [28] and are useful for measuring sniffing on a temporary basis in other large animals.

Nasal thermocouple and nasal pressure sensor

The most precise methods to date to measure sniffing involve direct intranasal measures through use of a temperature probe, called a thermocouple, or a pressure sensor. These can be inserted temporarily into the nares or implanted surgically. [4] [6] The basic principles of operation are shared between the temperature and pressure devices. Inhalation of ambient air provides cool temperature into the nasal cavity, whereas exhalation of inhaled air provides warm temperature into the nasal cavity and simultaneously an increase in intranasal pressure as air from the lungs is forced out of the nostrils. Placement of these sensors close to the olfactory epithelium of animals allows measures of odorized air transients as they reach the olfactory receptors [4] [29] and thus are common methods for measuring sniffing in the context of sensory neuroscience and psychological studies.

Sniffing in small animals

The earliest published study of sniffing behavior in small animals was performed in laboratory rats using video-based measures. [1] In this study robust changes in respiratory frequency were reported to occur during exploration of an open arena and novel odors. Resting respiration occurs ~2 times/second (Hz), and increases to about 12 Hz are noted during states of exploration and arousal. Similar transitions in sniffing frequency are observed in freely exploring mice, [3] which, however, maintain generally higher sniffing frequencies than rats (3 [rest] to 15 Hz [exploration] vs 2 to 12 Hz).

Transitions in sniffing frequency are observed in animals performing odor-guided tasks. Studies of recording sniffing in the context of odor-guided tasks involve implanting intranasal temperature and pressure sensors into the nasal cavity of animals and either measuring odor-orienting responses (fast sniffing) [29] or sniffing during performance in operant odor-guided tasks. [3] [4] [30] [31] Alternatively, animals can be conditioned to insert their snouts into an air-tight chamber with a pressure transducer embedded within to access nasal transients, while simultaneously odors are presented to measure responses while nose-poking. [2]

Notably, several studies have reported that modulation in sniffing frequency may be just as great in context of anticipation of odor sampling as during sampling of odors. [18] [31] Similar changes in sniffing frequency are even seen in animals presented with novel auditory stimuli, [32] suggesting a relationship between sniffing and arousal.

Sniffing in semi-aquatic animals

While sniffing is generally thought to occur solely in terrestrial animals, semi-aquatic rodents (American water shrew) also display sniffing behaviors during underwater odor-guided tasks. [20] Shrews inhale-exhale small amounts of air in a precise and coordinated fashion while tracking an underwater odor trail. This occurs through the inhalation of air above ground, to allow air to volatilize odors in an environment otherwise void of air.

Sniffing and control of odor input to the brain

Measurements of sniffing simultaneously with physiological measures from olfactory centers in the brain have provided information on how sniffing modulates the access and processing of odors at the neural level. Inhalation is necessary for odor input to the brain. [29] Further, odor input through the brain is temporally linked to the respiratory cycle, with bouts of activity occurring with each inhalation. [26] This linkage between sniffing frequency and odor processing provides a mechanism for the control of odor input into the brain by respiratory frequency [4] and possibly amplitude, though this is not well established.

Sniffing in humans

The nature of sniffing regulates odor perception in humans [7] [23] and in fact, in humans, a single sniff is often sufficient for optimal odor perception. [33] For instance, a deep, steady inhalation of a faint odor allows a more potent percept than a shallow inhalation. Similarly, more frequent sniffs provide a faster percept of the odor environment than only sniffing once every 3 seconds. These examples have been supported by empirical studies (see above) and have provided insights into methods whereby humans may change their sniffing strategies to modulate odor perception. [7] [23] [33]

Odor inhalation evokes activity throughout olfactory structures in humans. [9] Neuroimaging studies lack resolution to determine the impacts of sniffing frequency on the structure of odor input through the brain, although imaging studies have revealed that the motor act of sniffing is anatomically independent of sniff-evoked odor perception. [9] Implications for this include the shared but distributed pathways for odor processing in the brain.

Neural control of sniffing

Sniffing is fundamentally controlled by respiratory centers in the brainstem, including the Pre-Botzinger complex which governs inhalation/exhalation patterns. [34] Activity from respiratory brain stem structures then modulates nervous activity to control lung contraction. To exert changes to respiration, and thereby evoke sniffing behavior, volitional centers in the cerebral cortex must stimulate brain stem structures. It is through this simple pathway that the decision to inhale or sniff may occur.

The rapid modulation of sniffing upon inhalation of a novel odor or an irritating odor is evidence for an "olfactomotor" loop in the brain. [10] [35] In this loop, novel odor-evoked sniffing behavior can occur rapidly upon perception of a novel odor, one of interest, or an odor which is aversive.

Relation of sniffing to other stimulus sampling behaviors

Sniffing, as an active sampling behavior, is often grouped along with other behaviors utilized to acquire sensory stimuli. For instance, sniffing has been compared to rapid eye movements, or saccades, in the ability for both methods to provide rapid "snapshots" of information to the brain. [12] This analogy, though, may be imprecise since small animals (e.g., mice) make odor-based decisions (through sniffing) while also making visual decisions, yet do not saccade. Sniffing is also fundamentally similar to active touch, including swiping ones finger along a surface to scan texture.

In part due to the interrelatedness of the respiratory brain stem structures with other central pattern generators responsible for governing some other active sampling behaviors, sniffing in animals often occurs at similar frequencies (2 to 12 Hz) and in a phasic relationship to the active sampling behaviors of whisking and licking. [1] Whisking and sniffing are tightly correlated in their occurrence, [1] with sniff inhalations occurring during whisker protraction. Due to the metabolic need to coordinate breathing and swallowing, small animals (rats and mice) often lick at similar frequencies of sniffing (4 to 8 Hz) and swallow in between inhalations or during brief periods of apnea (cessation of breathing). [36]

Relevance to neurological disorders

Few studies have explored the impact of neurological disorders on sniffing behavior, although numerous neurological disorders affect respiration. Humans with Parkinson's disease have abnormal sniffing capabilities (i.e., reduced volume and flow rate) which may underlie olfactory perceptual impairments in the disease. [14] Studies into sniffing in mouse models of Alzheimer's disease [15] and also humans [37] have not found major effects of Alzheimer's pathology on both basal respiration and odor-evoked sniffing.

See also

Related Research Articles

<span class="mw-page-title-main">Olfactory nerve</span> Cranial nerve I, for smelling

The olfactory nerve, also known as the first cranial nerve, cranial nerve I, or simply CN I, is a cranial nerve that contains sensory nerve fibers relating to the sense of smell.

<span class="mw-page-title-main">Vomeronasal organ</span> Smell sense organ above the roof of the mouth

The vomeronasal organ (VNO), or Jacobson's organ, is the paired auxiliary olfactory (smell) sense organ located in the soft tissue of the nasal septum, in the nasal cavity just above the roof of the mouth in various tetrapods. The name is derived from the fact that it lies adjacent to the unpaired vomer bone in the nasal septum. It is present and functional in all snakes and lizards, and in many mammals, including cats, dogs, cattle, pigs, and some primates. Some humans may have physical remnants of a VNO, but it is vestigial and non-functional.

<span class="mw-page-title-main">Olfactory bulb</span> Neural structure

The olfactory bulb is a neural structure of the vertebrate forebrain involved in olfaction, the sense of smell. It sends olfactory information to be further processed in the amygdala, the orbitofrontal cortex (OFC) and the hippocampus where it plays a role in emotion, memory and learning. The bulb is divided into two distinct structures: the main olfactory bulb and the accessory olfactory bulb. The main olfactory bulb connects to the amygdala via the piriform cortex of the primary olfactory cortex and directly projects from the main olfactory bulb to specific amygdala areas. The accessory olfactory bulb resides on the dorsal-posterior region of the main olfactory bulb and forms a parallel pathway. Destruction of the olfactory bulb results in ipsilateral anosmia, while irritative lesions of the uncus can result in olfactory and gustatory hallucinations.

<span class="mw-page-title-main">Exhalation</span> Flow of the respiratory current out of an organism

Exhalation is the flow of the breath out of an organism. In animals, it is the movement of air from the lungs out of the airways, to the external environment during breathing. This happens due to elastic properties of the lungs, as well as the internal intercostal muscles which lower the rib cage and decrease thoracic volume. As the thoracic diaphragm relaxes during exhalation it causes the tissue it has depressed to rise superiorly and put pressure on the lungs to expel the air. During forced exhalation, as when blowing out a candle, expiratory muscles including the abdominal muscles and internal intercostal muscles generate abdominal and thoracic pressure, which forces air out of the lungs.

A chemoreceptor, also known as chemosensor, is a specialized sensory receptor which transduces a chemical substance to generate a biological signal. This signal may be in the form of an action potential, if the chemoreceptor is a neuron, or in the form of a neurotransmitter that can activate a nerve fiber if the chemoreceptor is a specialized cell, such as taste receptors, or an internal peripheral chemoreceptor, such as the carotid bodies. In physiology, a chemoreceptor detects changes in the normal environment, such as an increase in blood levels of carbon dioxide (hypercapnia) or a decrease in blood levels of oxygen (hypoxia), and transmits that information to the central nervous system which engages body responses to restore homeostasis.

Stimulus modality, also called sensory modality, is one aspect of a stimulus or what is perceived after a stimulus. For example, the temperature modality is registered after heat or cold stimulate a receptor. Some sensory modalities include: light, sound, temperature, taste, pressure, and smell. The type and location of the sensory receptor activated by the stimulus plays the primary role in coding the sensation. All sensory modalities work together to heighten stimuli sensation when necessary.

<span class="mw-page-title-main">Olfactory system</span> Sensory system used for smelling

The olfactory system or sense of smell is the sensory system used for smelling (olfaction). Olfaction is one of the special senses, that have directly associated specific organs. Most mammals and reptiles have a main olfactory system and an accessory olfactory system. The main olfactory system detects airborne substances, while the accessory system senses fluid-phase stimuli.

<span class="mw-page-title-main">Glomerulus (olfaction)</span>

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<span class="mw-page-title-main">Olfactory receptor</span> Chemoreceptors expressed in cell membranes of olfactory receptor neurons

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<span class="mw-page-title-main">Olfactory tubercle</span> Area at the bottom of the forebrain

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Olfactory fatigue, also known as odor fatigue, olfactory adaptation, and noseblindness, is the temporary, normal inability to distinguish a particular odor after a prolonged exposure to that airborne compound. For example, when entering a restaurant initially the odor of food is often perceived as being very strong, but after time the awareness of the odor normally fades to the point where the smell is not perceptible or is much weaker. After leaving the area of high odor, the sensitivity is restored with time. Anosmia is the permanent loss of the sense of smell, and is different from olfactory fatigue.

Dysosmia is a disorder described as any qualitative alteration or distortion of the perception of smell. Qualitative alterations differ from quantitative alterations, which include anosmia and hyposmia. Dysosmia can be classified as either parosmia or phantosmia. Parosmia is a distortion in the perception of an odorant. Odorants smell different from what one remembers. Phantosmia is the perception of an odor when no odorant is present. The cause of dysosmia still remains a theory. It is typically considered a neurological disorder and clinical associations with the disorder have been made. Most cases are described as idiopathic and the main antecedents related to parosmia are URTIs, head trauma, and nasal and paranasal sinus disease. Dysosmia tends to go away on its own but there are options for treatment for patients that want immediate relief.

<span class="mw-page-title-main">Odor</span> Volatile chemical compounds perceived by the sense of smell

An odor or odour is caused by one or more volatilized chemical compounds that are generally found in low concentrations that humans and many animals can perceive via their sense of smell. An odor is also called a "smell" or a "scent", which can refer to either an unpleasant or a pleasant odor.

<span class="mw-page-title-main">Sense of smell</span> Sense that detects smells

The sense of smell, or olfaction, is the special sense through which smells are perceived. The sense of smell has many functions, including detecting desirable foods, hazards, and pheromones, and plays a role in taste.

Olfactory memory refers to the recollection of odors. Studies have found various characteristics of common memories of odor memory including persistence and high resistance to interference. Explicit memory is typically the form focused on in the studies of olfactory memory, though implicit forms of memory certainly supply distinct contributions to the understanding of odors and memories of them. Research has demonstrated that the changes to the olfactory bulb and main olfactory system following birth are extremely important and influential for maternal behavior. Mammalian olfactory cues play an important role in the coordination of the mother infant bond, and the following normal development of the offspring. Maternal breast odors are individually distinctive, and provide a basis for recognition of the mother by her offspring.

<span class="mw-page-title-main">Insect olfaction</span> Function of chemical receptors

Insect olfaction refers to the function of chemical receptors that enable insects to detect and identify volatile compounds for foraging, predator avoidance, finding mating partners and locating oviposition habitats. Thus, it is the most important sensation for insects. Most important insect behaviors must be timed perfectly which is dependent on what they smell and when they smell it. For example, olfaction is essential for locating host plants and hunting prey in many species of insects, such as the moth Deilephila elpenor and the wasp Polybia sericea, respectively.

Retronasal smell, retronasal olfaction, is the ability to perceive flavor dimensions of foods and drinks. Retronasal smell is a sensory modality that produces flavor. It is best described as a combination of traditional smell and taste modalities. Retronasal smell creates flavor from smell molecules in foods or drinks shunting up through the nasal passages as one is chewing. When people use the term "smell", they are usually referring to "orthonasal smell", or the perception of smell molecules that enter directly through the nose and up the nasal passages. Retronasal smell is critical for experiencing the flavor of foods and drinks. Flavor should be contrasted with taste, which refers to five specific dimensions: (1) sweet, (2) salty, (3) bitter, (4) sour, and (5) umami. Perceiving anything beyond these five dimensions, such as distinguishing the flavor of an apple from a pear for example, requires the sense of retronasal smell.

<span class="mw-page-title-main">Dog sense of smell</span> Olfactory sensory system

The dog sense of smell is the most powerful sense of this species, the olfactory system of canines being much more complex and developed than that of humans. It is believed to be up to 10 million times as sensitive as a human's in specialized breeds. Dogs have roughly forty times more smell-sensitive receptors than humans, ranging from about 125 million to nearly 300 million in some dog breeds, such as bloodhounds. These receptors are spread over an area about the size of a pocket handkerchief. Dogs' sense of smell also includes the use of the vomeronasal organ, which is used primarily for social interactions.

<span class="mw-page-title-main">Olfactic communication</span> Social interaction through smell

Olfactic communication is a channel of nonverbal communication referring to the various ways people and animals communicate and engage in social interaction through their sense of smell. Our human olfactory sense is one of the most phylogenetically primitive and emotionally intimate of the five senses; the sensation of smell is thought to be the most matured and developed human sense.

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